Integrated analysis of metabolome, transcriptome, and bioclimatic factors of Acer truncatum seeds reveals key candidate genes related to unsaturated fatty acid biosynthesis, and potentially optimal production area

Background Lipids found in plant seeds are essential for controlling seed dormancy, dispersal, and defenses against biotic and abiotic stress. Additionally, these lipids provide nutrition and energy and are therefore important to the human diet as edible oils. Acer truncatum, which belongs to the Aceaceae family, is widely cultivated around the world for its ornamental value. Further because its seed oil is rich in unsaturated fatty acids (UFAs)- i.e. α-linolenic acid (ALA) and nervonic acid (NA)- and because it has been validated as a new food resource in China, the importance of A. truncatum has greatly risen. However, it remains unknown how UFAs are biosynthesized during the growth season, to what extent environmental factors impact their content, and what areas are potentially optimal for their production. Results In this study, transcriptome and metabolome of A. truncatum seeds at three representative developmental stages was used to find the accumulation patterns of all major FAs. Cumulatively, 966 metabolites and 87,343 unigenes were detected; the differential expressed unigenes and metabolites were compared between stages as follows: stage 1 vs. 2, stage 1 vs. 3, and stage 2 vs. 3 seeds, respectively. Moreover, 13 fatty acid desaturases (FADs) and 20 β-ketoacyl-CoA synthases (KCSs) were identified, among which the expression level of FAD3 (Cluster-7222.41455) and KCS20 (Cluster-7222.40643) were consistent with the metabolic results of ALA and NA, respectively. Upon analysis of the geographical origin-affected diversity from 17 various locations, we found significant variation in phenotypes and UFA content. Notably, in this study we found that 7 bioclimatic variables showed considerable influence on FAs contents in A. truncatum seeds oil, suggesting their significance as critical environmental parameters. Ultimately, we developed a model for potentially ecological suitable regions in China. Conclusion This study provides a comprehensive understanding of the relationship between metabolome and transcriptome in A. truncatum at various developmental stages of seeds and a new strategy to enhance seed FA content, especially ALA and NA. This is particularly significant in meeting the increasing demands for high-quality edible oil for human consumption. The study offers a scientific basis for A. truncatum’s novel utilization as a woody vegetable oil rather than an ornamental plant, potentially expanding its cultivation worldwide. Supplementary Information The online version contains supplementary material available at 10.1186/s12870-024-04936-6.


Supporting Information
Table S1.The total number of differential metabolites and differentially expressed genes at three developmental stages of A. truncatum seed.
Table S2.The transcriptome basic data of A. truncatum seeds at three developmental stages.
Table S3.The expression levels of FADs of A. truncatum seeds at three developmental stages.
Table S4.The expression levels of KCSs of A. truncatum seeds at three developmental stages.
Table S5.Location of the A. truncatum seed collected from 17 production areas.
Table S6.The seed morphological characteristics of the A. truncatum from 17 sampling locations.
Table S7.Relative content of eight main fatty acids in A. truncatum seed from 17 different sampling locations.
Table S8.Nineteen bioclimatic variables used in this study and their percent contribution.
Table S9.The primers used in RT-qPCR.Notice: data were represented as mean of three different determinations ± SD.Different tiny letters in the same row indicate significant differences of P < 0.05.Notice: results with r > 0.8 were marked by bold fonts.

Figure S3 .
Figure S3.KEGG enrichment analysis of DMs from metabolome at three developmental stages of A. truncatum seed.

Figure S4 .
Figure S4.KEGG enrichment analysis of DEGs from transcriptome at three developmental stages of A. truncatum seed.

Figure S5 .
Figure S5.Relative expression patterns of four genes of A. truncatum seed at three developmental stages detected by RNA-seq and RT-qPCR.

Figure S6 .
Figure S6.KEGG pathways jointly enriched from DMs and DEGs in stage 1 vs 2 and stage 1 vs 3 of A. truncatum seed.

Figure S7 .
Figure S7.Correlation heatmap of all the DMs and DEGs in stage 1 vs 2 and stage 1 vs 3 of A. truncatum seed.

Figure S8 .
Figure S8.Testing and training AUC values of ten-fold cross-validation models.

Figure S1 .
Figure S1.Heatmap of relative metabolites contents.X-axis indicates the sample name and the y-axis are the metabolites.Group indicates sample groups.The different colors are the results after standardization of the relative contents.S1, stage 1; S2, stage 2; S3, stage 3.

Figure S3 .
Figure S3.KEGG enrichment analysis of DMs from metabolome at three developmental stages of A. truncatum seed.KEGG pathway enrichment showed that DMs in (A) stage 1 vs 2, (B) stage 1 vs 3, and (C) stage 2 vs 3 seeds.

Figure S4 .
Figure S4.KEGG enrichment analysis of DEGs from transcriptome at three developmental stages of A. truncatum seed.KEGG pathway enrichment showed that DEGs in (A) stage 1 vs 2, (B) stage 1 vs 3, and (C) stage 2 vs 3 seeds.

Figure S5 .
Figure S5.Relative expression patterns of four genes of A. truncatum seed at three developmental stages detected by RNA-seq (left) and RT-qPCR (right).Four genes were randomly selected from FADs and KCSs, which were increased (Cluster-7222.41384 and Cluster-7222.21727)or decreased (Cluster-7222.39316 and Cluster-7222.40023)its expression during seed development.The mean values ± SD are shown from three biological replicates (n = 3).Different letters above the columns represent statistically significant differences according to one-way ANOVA with Tukey's multiple comparisons test (P < 0.05).R refers to the correlation analysis between transcriptome data and RT-qPCR data was implemented with the default arguments and Pearson correlation coefficient to evaluate statistical significance (**, P < 0.01).

Figure S6 .
Figure S6.KEGG pathways jointly enriched from DMs and DEGs in (A) stage 1 vs 2 and (B) stage 1 vs 3 of A. truncatum seed.

Figure S7 .
Figure S7.Correlation heatmap of all the DMs (top) and DEGs (left) in (A) stage 1 vs 2 and (B) stage 1 vs 3 of A. truncatum seed.the red indicates the positive correlation and green indicates the negative correlation.

Figure S8 .
Figure S8.Testing and training AUC values of ten-fold cross-validation models.One to ten represented the model code, ascending in order by testing AUC value.The mean testing and training AUC values were 0.879 and 0.902, respectively.

Table S10 .
The latitude and longitude details for recorded locations.